ORIGINAL ARTICLE

Utility of panoramic radiography for

identication of the pubertal growth period
Luciana Ja
come Lopes,a Thiago de Oliveira Gamba,a Maria Augusta Portella Guedes Visconti,b
Glaucia Maria Bovi Ambrosano,c Francisco Haiter-Neto,d and Deborah Queiroz Freitasd
S~ao Paulo and Rio de Janeiro, Brazil

Introduction: Our aim in this study was to investigate the association between dental mineralization stages and
the periods of the pubertal growth spurt (PGS). Methods: The sample included panoramic and hand-wrist
radiographs from 491 subjects (222 boys, 269 girls) aged 7 to 17 years. Dental development was rated, and
skeletal maturation was evaluated. The relevant associations were investigated by analysis of ordinal
multinomial logistic regression. Results: The second molar (odds ratio [OR] 5 4.34) and the rst premolar
(OR 5 2.45) were the best growth predictors for girls. For boys, the second molar (OR 5 6.80), second premolar
(OR 5 2.41), and canine (OR 5 3.21) proved to be the best predictors. Stages D and E of the second molar for
girls, and stages E and F for boys, corresponded to the onset of the accelerated growth spurt. Stage F of the
second molar for girls and stage G for boys corresponded to the peak of the PGS. At the end of the PGS,
most teeth had already attained apical closure. In girls, however, most second molars were found at stage G.
Conclusions: An association exists between the dental mineralization stages and the periods of the PGS, espe-
cially for second molars. Panoramic radiographs can be used as the rst diagnostic tool to estimate the pubertal
growth period. (Am J Orthod Dentofacial Orthop 2016;149:509-15)

I
t is well known that treatment timing plays an
important role in the results of nearly all dentofacial
orthopedic treatments for dentoskeletal dishar-
monies in growing patients.1 The skeletal maturation
status of a child aids in evaluating how much growth still
remains and whether the pubertal growth spurt (PGS)
has been reached or completed. Because of variations
in the timing of the PGS, chronologic age is not a valid
indicator of skeletal maturation.2,3 However, the
concepts of biologic or physiologic age have been
proposed previously. Biologic age is based on the
degree of maturation of different tissue systems that
a
Postgraduate student, Department of Oral Diagnosis, Oral Radiology Area, Pira-
cicaba Dental School, University of Campinas, S~ao Paulo, Brazil.
b
Associate professor, Department of Oral Diagnosis, Oral Radiology Area, Rio de
Janeiro Dental School, University of Rio de Janeiro, Rio de Janeiro, Brazil.
c
Professor, Department of Community Dentistry, Piracicaba Dental School, Uni-
versity of Campinas, S~ao Paulo, Brazil.
d
Professor, Department of Oral Diagnosis, Piracicaba Dental School, University of
Campinas, S~ao Paulo, Brazil.
All authors have completed and submitted the ICMJE Form for Disclosure of
Potential Conicts of Interest, and none were reported.
Address correspondence to: Luciana J
acome Lopes, Faculdade de Odontologia de
Piracicaba, Universidade de Campinas, Departamento de Diagn
ostico Oral, Av.
Limeira, 901, Caixa Postal 52, Piracicaba 13414-903, S~ao Paulo, Brazil;
e-mail, lu_jacome@hotmail.com.
Submitted, April 2015; revised and accepted, June 2015.
0889-5406/$36.00
Copyright 2016 by the American Association of Orthodontists.
http://dx.doi.org/10.1016/j.ajodo.2015.06.030
can be estimated by somatic, sexual, skeletal, and
dental maturation.2,4
The assessment of skeletal maturation consists of the
visual inspection of developing bones: various ossica-
tion centers of the skeleton, such as the hand and wrist,
foot, ankle, hip, elbow, and cervical vertebrae, can be
used.5 Skeletal development has most commonly been
determined using hand-wrist radiographs6-8 and lateral
cephalograms.1,9 However, the use of such radiographs
has been questioned because of radiation hygiene and
safety problems, in that it requires patients to have
additional radiographs.2
Dental maturation detected with radiographic
methods has been reported to be a potential predictor
of skeletal maturation.3,5,10-13 The ability to recognize
dental development stages through the examination of
periapical or panoramic radiographs by most
orthodontic or pediatric dental practices is a key
reason that studies should attempt to assess
physiologic maturation without resorting to hand-
wrist radiographs.3 Moreover, no additional exposure
to radiation would be necessary if the periods of the
PGS were identied through panoramic radiographs (a
commonly requested diagnostic radiograph), bearing
in mind the as low as reasonably achievable principle.
Growth and development of children and adolescents
are inuenced by ethnic origin, climate, nutrition, socio-
economic level, and urbanization.14 In spite of all these
509
510
causative factors of variations in the timing of the PGS,
high correlations have been reported between dental and
skeletal maturation.2,3,5,10-13,15 However, a high
correlation is a natural tendency because both are in
progress. A high correlation coefcient does not
provide information about whether the dental
maturation stage is satisfactory for diagnostic
identication of the skeletal maturation stage.16,17
Moreover, a high correlation coefcient does not
identify which teeth and their mineralization stages are
associated with skeletal maturation. Therefore, it is
important to identify the teeth and the corresponding
mineralization stages related to the different stages of
maturation.
The aim of this study was to identify the pubertal
growth period with the dental mineralization stages us-
ing panoramic radiographs, which should lead to a
reduction in the number of radiographs needed during
treatment and benet the patients economically. The
best predictor teeth were identied.
MATERIAL AND METHODS
This cross-sectional study included both panoramic
and hand-wrist radiographs of 491 subjects (222 boys,
269 girls) selected from the database of an oral radiology
clinic in Piracicaba, Brazil. All radiographs were obtained
with the same equipment.
The selection criteria included (1) chronologic age
from 7 to 17 years; (2) white ethnicity and well nourished
and free of serious illness; (3) no abnormal dental condi-
tions, such as impaction, transposition, and congenitally
missing teeth; (4) no history of trauma or disease to the
face and the hand-wrist regions; (5) no previous ortho-
dontic treatment; (6) no permanent teeth extracted; and
(7) both images (panoramic and hand-wrist radiographs)
taken at the same time.
Subjects who had not started the maturation process
were excluded.
All radiographs were assessed using Windows Photo
Viewer (Microsoft, Redmond, Wash) on a notebook
with a light-emitting diode 14.0-in high-denition
screen (1366 3 768 pixels) (Dell, Round Rock, Tex), by
2 calibrated oral radiologists (L.J.L, T.O.G.) under dim
light conditions. The observers were allowed to use the
zoom tool and to change the brightness and contrast
of the images. When a consensus could not be reached
between the 2 examiners, a third radiologist (D.Q.F.) as-
sisted in making the decision. The assessment of each
imaging modality (panoramic and hand-wrist radio-
graphs) was performed separately.
Tooth mineralization was rated according to the
method described by Demirjian et al18 in which 1 of
the 8 stages of mineralization (A-H) was assigned for
April 2016  Vol 149  Issue 4 American Journal of Orthodontics and Dentofacial Orthopedics
Lopes et al
each tooth (Fig). In this study, the examined teeth
included the mandibular left canine, rst and second
premolars, and second molar. In case of any missing
mandibular left teeth, the mandibular right teeth that
corresponded to the missing teeth were examined.
Skeletal maturation was assessed according to the
method described by Grave and Brown.6 This method in-
cludes 14 stages of bone ossication, which represent 3
growth periods: the onset, the peak, and the end of PGS
(Table I).
Statistical analysis
The statistical analyses were performed using soft-
ware (version 9.2; SAS, Cary, NC). The signicance level
was set at 5%. The analyses were the following.
1. The means of the chronologic ages for both sexes in
the 3 periods of skeletal maturation were compared
by 2-way analysis of variance (ANOVA) and the post
hoc Tukey test.
2. The analysis of ordinal multinomial logistic regres-
sion evaluated which teeth had mineralization asso-
ciated with skeletal maturation. This analysis is used
when studying a categorical dependent variable
with more than 2 ordinal responses.19 The use of
the logistic model for ordinal responses has a simple
interpretation and greater power. The quality of the
models' adjustments was analyzed by the log of
likelihood ratios and the Akaike information crite-
rion (AIC). It estimates the quality of each model;
the adjusted model with the lowest value of log-
likelihood ratios and AIC are selected. Lower values
indicate higher quality and therefore better models.
3. The percentages of the distribution of the stages of
mineralization for each tooth were calculated to
study the relationships between the stages of miner-
alization of the teeth and skeletal maturation.
RESULTS
Table II shows the distributions of the mean chrono-
logic ages and sexes of the sample. ANOVA showed dif-
ferences between the sexes (P \0.05) and between the
skeletal maturation periods (P \0.05). A consistently
earlier occurrence for each skeletal maturation stage
was observed more often in the girls than in the boys.
The mean chronologic age of the girls was approxi-
mately 1.8 years (range, 1.7-2.0 years) younger than
that of the boys.
The ordinal multinomial logistic regression analyses
between the skeletal maturation stages and the mineral-
ization stages of the teeth are presented in Table III for
girls and Table IV for boys. The analysis of ordinal
Lopes et al
Fig. Reinterpretation of the dental mineralization stages proposed by Demirjian et al.18
multinomial logistic regression predicts the odds ratio
(OR) of the tooth to predict the pubertal growth period
(onset, peak, and end) by the mineralization stages. The
mineralization stage of the teeth is the predictor,
whereas the skeletal maturation stage is the dependent
variable. According to the results, the second molar and
the rst premolar were statistically signicant as pre-
dictors of the maturation stages for girls (P \0.05).
When the estimated values were analyzed, we observed
that the second molar had the highest value (1.47),
which signies more inuence in predicting the skeletal
maturation. In accordance, the point estimation for the
OR was highest in the second molar (OR 5 4.34; 95%
condence interval [CI]: 2.64-7.68); ie, the
second molar has 4.34 times more chance that its
mineralization stages will predict the skeletal matura-
tion stage than the other teeth. However, considering
the 95% CI for the OR, no signicant difference could
be identied between the rst premolar and the
second molar. For the other studied teeth (canine and
second premolar), ORs were not found because they
were not statistically signicant as predictors
(P .0.05).
American Journal of Orthodontics and Dentofacial Orthopedics
511
Similarly, the second molar had the highest estimated
value (1.92) and OR values (OR 5 6.80, 95% CI: 3.48-
13.27) in boys, but the canines and the second premolars
can also be used as predictors of skeletal maturation
(P \0.05). This OR value signies that the
second molar has a 6.8 times greater chance that its
mineralization stages will predict the skeletal maturation
stage than other teeth. For boys, only the rst premolar
was not a predictor of the maturation stage (P .0.05).
Differences were observed between the sexes in the
pattern of mineralization of the various teeth. Tables V
through VII show the percentages of the distributions
of each tooth in the 3 skeletal maturation periods.
At the onset, a wide distribution of mineralization
stages was seen in all teeth of both sexes. Considering
the most reliable tooth predictors for skeletal maturation
in girls, most rst premolars were identied in stage E or
F; for the second molar, they were found in stage D or E.
For boys, most second molars were observed in stage E
or F, whereas canines and premolars were found in stage
F or G.
At the peak, most teeth were identied in the
advanced stages (G and H) of dental mineralization
April 2016  Vol 149  Issue 4
512
Table I. Description of the ossication events
Stage Ossication events
Onset
1 Proximal phalanx of the second nger; epiphysis is as wide as
its diaphysis
2 Middle phalanx of the third nger; epiphysis is as wide as its
diaphysis
3 Hooking of hamate: stage 1
4 Appearance of pisiform
5 Radius; epiphysis is as wide as its diaphysis
Peak
6 Appearance of ulnar sesamoid at metacarpophalangeal joint
of the rst nger
7 Hooking of hamate: stage 2
8 Middle phalanx of the third nger; epiphysis caps its
diaphysis
9 Proximal phalanx of the rst nger; epiphysis caps its
diaphysis
10 Radius; epiphysis caps its diaphysis
End
11 Distal phalanx of the third nger; complete epiphyseal union
12 Proximal phalanx of the third nger; complete epiphyseal
union
13 Middle phalanx of the third nger; complete epiphyseal
union
14 Radius; complete epiphyseal union
(Table VI). Again, considering the most reliable tooth
predictors for skeletal maturation in girls, the minerali-
zation stages F and G appeared mostly in the
second molars; in the rst premolars, stages G and H
were the most common. In most of the boys, stage G
was identied in the second molar; in the second premo-
lar, stages G and H were predominant, whereas the ca-
nines were more commonly in stage H.
At the end of the PGS, root formation of the teeth
was deemed complete in all boys and in most girls
(Table VII). The second premolar and the second molar
in boys were also predominant in stage H. The develop-
ment of the second premolar and the second molar for
girls became highly dense in stages H and G, respectively.
In general, the tooth mineralization stages in boys
tended to be more advanced when compared with those
of the girls in the same skeletal maturation period.
DISCUSSION
Relationships between the mineralization stages of
individual teeth and skeletal maturation have been pre-
viously reported in the literature.3,5,11,14,15,20 Most
authors found high correlations between dental
mineralization stages and skeletal maturation, as
expected.3,5-11,15-18,21 This can be explained by the
progressive growth and development of each patient,
as well as his or her dental and skeletal maturation. In
this way, to our knowledge, this is the rst study to
April 2016  Vol 149  Issue 4 American Journal of Orthodontics and Dentofacial Orthopedics
Lopes et al
Table II. Distribution of chronologic ages for all sub-
jects grouped by skeletal maturation
Number of
subjects Chronologic age (y), mean (SD)
Maturation
event Male Female Male Female
Onset 61 50 11.04 (0.87)Ac 8.99 (0.78)Bc
Peak 92 105 12.72 (1.02)Ab 11.02 (1.24)Bb
End 69 114 15.26 (0.97)Aa 13.40 (1.30)Ba
Different letters (uppercase in the horizontal and lowercase in the
vertical) indicate statistically signicant differences (P \0.05), ac-
cording to the Tukey test.
statistically analyze and evaluate which teeth and
mineralization stages are the best predictors for the
maturation stages; we found that the second molars
are the best predictors for both sexes.
Establishing an accurate evaluation of the develop-
mental stage is a key element in the proper diagnosis
and treatment of pediatric patients. The optimal treat-
ment time for dentofacial orthopedics is intimately
related to the identication of periods of accelerated
growth that can contribute signicantly to the correc-
tion of skeletal disharmonies in each patient. Because
of variations in factors such as sex, race, and environ-
ment, chronologic age is unreliable for the prediction
of human growth and development.2,16 Thus, dental
maturation has been considered to be a useful method
in predicting the PGS.5,10,12
The ability to recognize dental development stages
and the evaluation of panoramic radiographs during
routine dental treatment is a practical reason for at-
tempting to assess physiologic maturation without re-
sorting to hand-wrist or lateral cephalometric
radiographs; this should lead to a reduction in the num-
ber of radiographs needed during the treatment.3
Different methods for evaluating dental and skeletal
maturation have resulted in discrepancies between
studies. Even a high correlation does not identify the
teeth whose mineralization stages are associated with
skeletal maturation. Thus, in this study, we sought to
analyze ordinal multinomial logistic regressions to
determine this association, which is a more adequate
analysis.
In this study, the mineralization stages of the teeth
were preferred to the eruption stages, because tooth for-
mation has been proposed as a more reliable criterion for
determining dental maturation.3,16,18,21 The method of
Demirjian et al18 was chosen because it is one of the
simplest, most practical, and widely used methods for
predicting dental development.22 In addition, the
pattern of development of the teeth does not vary
much in different populations; differences arise only
Lopes et al 513

Table III. Results of ordinal multinomial logistic regression analysis* for girls
Variable Estimate SE Wald chi-square P value OR 95% CI
First premolar 0.90 0.28 9.88 0.0017 2.45 1.40-4.28
Second molar 1.47 0.29 25.48 \0.0001 4.34 2.46-7.68
Intercept (1) 12.78 1.36 88.43 \0.0001
Intercept (2) 16.86 1.69 99.76 \0.0001
AIC intercept only 5 565.57; AIC intercept and covariates 5 347.69; 2 log-likelihood intercept only 5 516.57; 2 log-likelihood intercept and
covariates 5 339.69.
*Mineralization stage of teeth was the predictor, and maturation stage was the dependent variable.

Table IV. Results of ordinal multinomial logistic regression analysis* for boys
Variable Estimate SE Wald chi-square P value OR 95% CI
Canine 1.17 0.43 7.31 0.0069 3.21 1.38-7.50
Second premolar 0.88 0.34 6.64 0.0100 2.41 1.24-4.43
Second molar 1.92 0.34 31.51 \0.0001 6.80 3.48-13.27
Intercept (1) 30.46 3.45 77.92 \0.0001
Intercept (2) 26.42 3.18 68.95 \0.0001

AIC intercept only 5 484.95; AIC intercept and covariates 5 274.99; 2 log-likelihood intercept only 5 480.95; 2 log-likelihood intercept and
covariates 5 264.99.
*Mineralization stage of teeth was the predictor, and maturation stage was the dependent variable.

when the pattern is converted to dental age. Hence, it is a
valid measurement instrument for universal use.18 Its
criteria consist of distinct details based on shapes and
proportions of root length, based on the relative value
to crown height rather than on absolute length. Further-
more, elongated or foreshortened projections of the
teeth will not affect the reliability of the assessment.
The skeletal maturation assessment was based on the
system of Grave and Brown,6 considered a simple
approach used to determine the degree of maturation.
To provide a reliable description relative to growth
stages because of small radiographic changes detected
from one event to another and to facilitate clear
discrimination between the stages, the 14 stages of
bone ossication are represented by the 3 growth pe-
riods: onset, peak, and end of the PGS.
The mean chronologic age for each growth period
indicated that the skeletal maturation stages occur
consistently earlier in girls than in boys; this nding
agreed with the information published in several
studies.2,3,13 The mean chronologic age of the girls was
approximately 1.8 years (range, 1.7-2.0 years) younger
than that of the boys. This is similar to that reported in
most publications, with an average of 1.5 years.5,13 The
skeletal maturation in this population as well as in
recent studies5,15 has happened earlier when compared
with the reference study.6
We found that boys tend to have more advanced
tooth development when compared with girls regarding
the skeletal maturation stages as shown in some
previous studies.5,11,12,15 This could be explained by
the later occurrence of skeletal maturation in boys
than in girls. Therefore, a sex distinction must be
contemplated when estimating facial growth according
to dental maturation.
The results support a signicant association between
the dental maturation stages of some teeth and the skel-
etal maturation periods; this can lead clinicians to iden-
tify the PGS with panoramic or intraoral radiographs.
The same can be observed in different popula-
tions.2,3,5,11,12,20,23-25 Other studies, however, have
reported a weak correlation between skeletal and
dental maturation.26-28 Recent studies, in spite of
showing a high correlation, suggest that the clinical
usefulness of the dental maturational stages for the
identication of individual skeletal maturation is
limited in both sexes.16,17 The absence of agreement
among studies can be justied by differences in the
methods used to evaluate dental and skeletal
maturation.3 Moreover, discrepancies in the number,
age, and racial background of the subjects, conditioned
by ethnic origin, climate, nutrition, socioeconomic sta-
tus, and industrialization, may be other reasons for var-
iable results.14
The second molar showed the highest association be-
tween skeletal maturation and mineralization stages of
the teeth for both sexes. According to Kumar et al,3
this tooth has an advantage over the other teeth because
its development tends to continue over a longer period
and until a later age. Apex closure generally extends

American Journal of Orthodontics and Dentofacial Orthopedics April 2016  Vol 149  Issue 4
514 Lopes et al

Table V. Distribution of mineralization stages of teeth at the onset of PGS

Canine First premolar Second premolar Second molar

Mineralization stage Female (%) Male (%) Female (%) Male (%) Female (%) Male (%) Female (%) Male (%)
D - - 2.00 - 4.00 - 32.00 1.64
E 4.00 - 46.00 3.28 58.00 14.75 54.00 26.23
F 62.00 37.70 40.00 42.62 32.00 54.10 10.00 47.54
G 24.00 47.55 10.00 45.90 6.00 27.87 4.00 24.59
H 10.00 14.75 2.00 8.20 - 3.28 - -

Table VI. Distribution of mineralization stages of teeth at the peak of PGS

Canine First premolar Second premolar Second molar

Mineralization stage Female (%) Male (%) Female (%) Male (%) Female (%) Male (%) Female (%) Male (%)
D - - - - 0.95 - 3.81 -
E - - 6.67 - 11.43 - 16.19 2.17
F 14.28 3.26 20.95 7.61 35.24 21.74 31.43 13.04
G 27.62 18.48 33.33 26.09 35.24 39.13 46.67 76.09
H 58.10 78.26 39.05 66.30 17.14 39.13 1.90 8.70

Table VII. Distribution of mineralization stages of teeth at the end of PGS

Canine First premolar Second premolar Second molar

Mineralization stage Female (%) Male (%) Female (%) Male (%) Female (%) Male (%) Female (%) Male (%)
D - - - - - - - -
E - - - - - - - -
F - - 0.88 - 2.64 - 6.14 -
G 2.63 - 9.65 - 35.96 1.45 61.40 26.09
H 97.37 100.00 89.47 100.00 61.40 98.55 32.46 73.91

up to 16 years of age in normal children. Similar results
were also found in Turkish subjects11,12 as well in
Chinese girls2 and Indian subjects.13 In contrast, a strong
correlation was found between the mineralization of the
mandibular canine and skeletal maturation in the
studies of Chertkow and Fatti23 and Coutinho et al.10
In Thai subjects, the premolars and the second molars
showed high correlations.5 The greatest association in
female Iranians also proved to be the second molar.20
A close comparison of the various studies is virtually
impossible because of many differences in methodolo-
gies, ages, sample sizes, and especially ethnicities.
The authors of some studies also found similar results
regarding the stages of dental mineralization and skeletal
maturation periods shown in Tables V through VII.
Coutinho et al10 and Krailassiri et al5 found that the ma-
jority of the canines in stage F were at the onset of the
PGS. This nding also suggests the beginning of the
PGS in our study. Stage G of the second molars for boys
was also related to the period of rapid growth in the nd-
ings of Krailassiri et al and Kumar et al.3 In contrast, this
previous study found delayed tooth development in girls
when compared with our study, since stage E of the
second molars indicated the peak of the PGS.
As a clinical implication from our study, the associa-
tion between the tooth mineralization stages and the
skeletal maturation indicators allows clinicians to easily
identify the pubertal growth period from the panoramic
or intraoral radiographs. In short, we found that the
second molar, stages D and E for girls and stages E
and F for boys, serves as a simple tool to evaluate the
onset of the accelerating growth period. The second
molar, stages F or G for girls and stage G for boys, indi-
cates a high rate of growth acceleration. However, stage
G for girls can also indicate the end of the PGS; there-
fore, the evaluation of this stage would not be useful
in estimating the skeletal maturation period, or it could
be used in association with H stage of the rst premolar.
CONCLUSIONS
An association exists between the dental mineraliza-
tion stages and the skeletal maturation periods in the
studied population. The mandibular second molar and
the mandibular rst premolar were the most reliable

April 2016  Vol 149  Issue 4 American Journal of Orthodontics and Dentofacial Orthopedics
Lopes et al
growth predictors for girls. For boys, who showed a more
advanced trend in tooth mineralization, the mandibular
second molar, mandibular second premolar, and
mandibular canine proved to be the most reliable predic-
tors. Hence, because the dental mineralization stages
can be used as a simple and useful measurement instru-
ment to estimate the skeletal maturation period, the
panoramic and intraoral radiographs can be used as
the rst diagnostic tool to estimate the skeletal matura-
tion period, reducing the requirement for hand-wrist ra-
diographs or suggesting the ideal time for their request.
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April 2016  Vol 149  Issue 4